Download rats given 13-aminopropionitrile or hydrocortisone using a time

European Journal of Orthodontics 19 (1997) 21 28
9 1997 European Orthodontic Society
In vitro measurement of orthodontic tooth movement in
rats given 13-aminopropionitrile or hydrocortisone using a
time-lapse videotape recorder
A. Yamane*, T. Fukui** and M. Chiba*
Departments of *Pharmacology and **Orthodontics, School of Dental Medicine, Tsurumi University,
Yokohama, Japan
SUMMARY In vitro tooth movement of rat molars in response to an orthodontic force was
recorded using a time-lapse videotape recorder and analysed by a computer system. Rats
received daily s.c. injections of 13-aminopropionitrile (BAPN, 300 mg/kg/day) or hydrocortisone (10 mg/kg/day) for a period of 7 days. After drug administration, the animals were killed
and the mandibles dissected. The jaw was then held under a stereomicroscope with a
haemostatic clamp and an elastic band was inserted between the first and second molars.
The movements of reference points on the occlusal surfaces of the first and second molars
were recorded for 20 hours using a time-lapse videotape recorder. Mesiolingual movement
of the first molar and distobuccal movement of the second molar were observed. During
the experimental period, the greatest amount of total tooth movement in the first and
second molars was seen in the group pretreated with BAPN, less movement was observed
in the control group, and the group pretreated with hydrocortisone exhibited the least
amount of movement. The highest rates of tooth movement were observed during the
initial hour in each of the groups, and decreased thereafter. The initial rates of movement
were also greatest in the BAPN group, less in the control group, and least in the hydrocortisone group. These results indicate that treatment with BAPN accelerated experimental tooth
movements in vitro and hydrocortisone treatment inhibited the movements, suggesting
that, although a part of the tooth movement measured in this experiment was due to
deformation of the alveolar bone, the mechanical properties of the periodontal ligament
play an important role in the regulation of orthodontic tooth movement.
Introduction
Previous research has shown that the mechanical response of connective tissues to applied
loads is closely related to the soluble or insoluble
collagen content of the tissues; the mechanical
strength is decreased by lathyrogens, inhibitors
of collagen cross-linking, and increased by glucocorticoids, which are known to decrease Ievels
of salt-soluble collagen (Vogel, 1971, 1974,
1975; Dombi et al., 1993).
The effects of lathyrogens, such as 13aminopropionitrile, aminoacetonitrile, and
hydrocortisone on the mechanical properties of
the periodontal ligament in rat incisors
(Ohshima, 1982; Yamaguchi, 1992), rat molars
(Ohkawa, 1982; Yumoto, 1986; Koizumi, 1986;
Ohshima et al., 1989; Kondo, 1991 ), and rabbit
incisors (Moxham and Berkovitz, 1984) have
been thoroughly examined. Changes in the soluble and insoluble collagen content of the periodontal ligament (in rat molars and incisors),
following the administration of lathyrogens,
have also been examined (Taverne et al., 1986).
Although orthodontic tooth movement is
affected by a number of factors, such as the
magnitude of the force applied (Reitan, 1960,
1964), duration of force application (Reitan,
1960, 1975), and the number and shape of roots
(Macapanpan et al., 1954), the mechanical
characteristics of the periodontal ligament are
thought to have the most profound effect.
Despite numerous studies of orthodontic tooth
movement, a detailed analysis of the effects of
periodontal ligaments with different mechanical
properties, produced experimentally by expo-
22
A. Y A M A N E ET A L .
sure to lathyrogens or glucocorticoids, on orthodontic tooth movement has yet to be performed.
Therefore, in the present study, in vitro tooth
movement, in the dissected jaws of rats which
had received daily injections of [3-aminopropionitrile or hydrocortisone, were recorded
during the application of an orthodontic force.
Materials and methods
Experimental anima&
Male Wistar rats (n--33), 7-8 weeks old,
with an average body weight of 2 1 9 + 9 g
(mean + 1SD) were divided into three groups of
9-12 animals each. The rats were given a powdered diet (CE-2; Clea Japan, Tokyo, Japan)
and water ad libitum during the experimental
period. One group of rats received daily s.c.
injections of 300 mg of ]3-aminopropionitrile
fumarate (BAPN) (Tokyo Kasei, Tokyo,
Japan) per kg of body weight, f o r a period of 7
days. A different group received daily s.c. injections of 10 mg of hydrocortisone acetate ( H C )
(Nippon Merck-Banyu, Tokyo, Japan) per kg
of body weight, also for a 7-day period. The
remaining group of rats received daily subcutaneous injections of the same volume
(0.2 mi/100 g body weight) of saline f o r a period
of 7 days (control group). At the end of the
experimental period, the animals were anaes-
~
I
Controller~
m Str erjj;p e
i
[Video tape I
recorder ]
_
thetized
with
ether
and
decapitated.
Immediately after death, the right mandibles
were dissected and the adhering soft tissues
removed.
Mandible immobilization and labelling of
reference points
The angular process of the dissected mandible
was held in place with a haemostatic clamp; the
tip of the clamp and the bone surface were
cemented together with self-curing resin. The
body of the clamp was fixed to the metal bar
of a magnetic stand (Fig. 1). The approximal
cusps of the first and second molars were flattened, using a dental diamond disc, and regions
on the surface were painted with oily marking
ink (Fig. 2) to provide clear reference points.
The mandible was placed in a small dish and
exposed to a continuous flow of phosphatebuffered saline containing antibiotics (50 units
of penicillin G and 50 ~tg of streptomycin/ml;
GIBCO, New York, USA), at a ¡
rate of
2 ml/h with a peristaltic pump. The experiment
was performed at room temperature, which
ranged from 23-27~
Recording of tooth movement with a time-lapse
videotape recorder
Two clear reference points were chosen, one on
the distal surface of the first molar and the
other on the mesial surface of the second molar,
TV camera
~0~ ]!
I
I 1
ooo
TV screen
Peristaltic
pump
/
I
Elastic
Dish
band
Magnetic
stand
Figure 1 Diagrammatic representation of the procedure used to record tooth movement in vitro. The angular process of
the mandible was attached to the haemostatic clamp. Pictures of the reference points were taken at hourly intervals with a
television camera set on a stereomicroscope and recorded using a time-lapse videotape recorder.
23
IN VITRO O R T H O D O N T I C TOOTH MOVEMENT
Buceal
i
M1
a.[
i
i
!
ao
~b.
M2" ~
.%4~,;~ ,n,
(Xo.Yo) ~
\
(B)
Lingual
Figure 2 (A) The occlusal surfaces of the right mandibular molars following the insertion of an elastic band (e). The
rectangle outlines the microscopic field. The lower margin of the microscopic field was set parallel to the midline of the
dental arch. Arrows show reference points (a) and (b) on the first and second molars, respectively. M 1, M2 and M3 represent
the first, second and third molars, respectively. (B) Diagrammatic representation showing the movement of the reference
points on the distat surface of the first molar and the mesial surface of the second molar. The rectangle outlines the
microscopic field, ao and b0 show the position of the reference point just before insertion of an elastic band and ah and b,
show the position of the reference point, n hours after insertion of an elastic band. Solid line shows the position of the first
and second molars just before insertion of an elastic band and dotted line shows the position of the first and second molars
n hours after insertion of an elastic band. M1 and M2 represent the first and second molars, respectively.
using a stereomicroscope (Fig. 2). The microscopic image was recorded at 1 hourly intervals
for 20hours, through a television camera
(C2400-77; Hamamatsu Photonics, Hamamatsu, Japan) positioned on the stereomicroscope, and linked to a time-lapse videotape
recorder (SIV-JS; Sankei, Tokyo, Japan).
Filming began after insertion of a latex elastic
band (No. 404-126; Unitek, Monrovia, CA,
USA), with an average thickness of 594 t.tm, in
the interproximal space between the right mandibular first and second molars. The lower
margin of the microscopic field was set parallel
to the midline of the dental arch; the rectangle
in Figure 2 depicts the microscopic field. The
period of time between the death of the animals
and the insertion of the elastic band was 88 _+ 12
minutes (mean_+ 1SD) in the control group,
86 + 10 minutes (mean_+ 1SD) in the HC group,
and 90_+ 25 minutes (mean_+ 1SD) in the BAPN
group.
Data analysis using an image analyser
The videotaped data were analysed using an
image analyser (Luzex 3U; Nikon, Tokyo,
Japan) linked to a personal computer
(PC9801N; NEC, Tokyo, Japan). The reference-point co-ordinates were first successively
measured at 1 hourly intervals. Then, referencepoint movements were depicted as traced lines
and values of tracings we~ cumulated with the
personal computer. Both the total amount of
movement (lam) and the rates of movement
(gm/h) were calculated for each reference point
as follows: The position (the co-ordinates) of
the reference point before band insertion was
24
A. YAMANE ET AL.
determined as position 0 (Xo, Yo) on the monitor
screen of the image analyser and the positions
after band insertion were determined as position
1 (xi, Yl), position 2 (x2, Y2), position n (xn, Yn)
etc. (Fig. 2B). The co-ordinates were stored in
the computer memory. The distance between
the two successive points was calculated by
using the co-ordinates. The cumulated distances
were regarded as the total amount of tooth
movement. The distance between the two successive points/hour was regarded as the rate of
tooth movement. The resolution was estimated
to be 2.5 lato.
Buccal
Saline M1
-~
Results
Table 1 shows the weights of animals, mandibles, and adrenal glands after daily injections
of saline, HC, or BAPN for a 7-day period.
Significant decreases were observed in the
weights of animals and adrenal glands in the
HC group (P<0.001) at the end of the experimental period, but weights in the BAPN group
remained stable. Mandible weights did not
undergo significant changes in any of the
groups.
Movement of the reference points on tooth
surfaces
Figure 3 shows tracings of the movement of
reference points on the surfaces of the first and
second molars of rats which had received daily
injections of saline, BAPN, or HC, during a
Table 1 The weights of animals, mandibles, and
adrenal glands after daily injections of hydrocortisone
or ]3-aminopropionitrile (BAPN). Data shown is the
mean_+ 1 SD for each group.
Animal (g)
Mandible (mg)
Adrenal gland (mg)
Control
(n=9)
Hydrocortisone
(n=12)
BAPN
(n=12)
252_+13
359_+16
25_+3
211+8"
357_+14
15_+2"
248_+10
358_+20
27_+3
*P<0.001 (significant difference between the control and
experimental groups)
~~-..._~--.~-~, 0 0 , - ~ ~ ~ ,
BAPN
. :_____~,o]oJ-J~ --Ÿ
HC
Statistical analysis
The differences of the mean values between the
control and BAPN groups, the control and HC
groups, and the BAPN and H C groups were
compared by Student's t-test.
M2
lOOpm
...~,._...~.~~"0 O . J - ~ :
300pm
300pm
lOOpm
Lingual
Figure 3 Movement of reference points on the tooth surfaces of the first and second molars of rats which had
received daily injections of saline, [3-aminopropionitrile
(BAPN), or hydrocortisone (HC). The movements are
depicted traced lines and were taken during a 20 hour
period following the insertion of an elastic band between
the teeth. The horizontal axis is parallel to the midline of
the dental arch. The position of the reference point before
band insertion is labelled as 0, and each point represents
the mean of data collected from 9-12 animals.
20 hour period following the insertion of an
elastic band between the teeth. Mesial movement of the first molars and distal movement
of the second molars was recorded in all of the
groups. However, the movements were not
parallel to the midline of the dental arch.
Lingual movement of the first molars and buccal
movement of the second molars (lateral movement) were also observed in each group. Tracing
lines depicting movement of the first and second
molars were not always straight, particularly in
the control and HC groups.
Amount of tooth movement
Figures 4 and 5 show the total amount of tooth
movement in the first (Fig. 4) and second
(Fig. 5) molars, following the insertion of an
elastic band between the teeth. In both the first
and second molars in each of the groups, tooth
movement was the most pronounced during the
initial hour of exposure to orthodontic force,
but all of the teeth continued to move throughout the experimental period. The average
25
IN VITRO ORTHODONTIC TOOTH MOVEMENT
,_,
400
-o-- Saline
-9
BAPN
-~
9 ,
First m o l a r
9
E.,
e-
~
3oo
*
,
*
,
*
,
*
* / t /k. =
0~ 9
,
_ o--o ~
O~.w~
::..:.-;'"o.o_O-O-~
o O
* .--" o. o-O
_o_~176
, :.,%..o
~.~_~176 ~
200
,_o...o
9
E
,
.
E
9
,
*
,~
O
**
,:*****
"*
** *
100
*/o
*
, ./,_o
9
o~'o ,"
__cr~--
OŸ 0
i0
;1~1
/
'~
o.~ ~
/
u/
I-0
0
I
I
5
10
'
I
I
15
20
Time after insertion of elastic band (hours)
Total movement (~tm) of the reference points in
the first molar, following the insertion of an elastic band
between the teeth, in rats which had received daily injections
of saline, 13-aminopropionitrile (BAPN) or hydrocortisone
(HC). The position of the reference point before band
insertion is labelled as 0. Each point represents the mean
of data collected from 9-12 animals. Significant differences
between the control and BAPN groups: * P < 0.05; between
the control and HC groups, ~ P < 0 . 0 5 ; and between the
BAPN and HC groups, **P<0.01, ***P<0.001.
Figure 4
Second
400
-o-- Saline
-9
BAPN
--a-- HC
molar
E
e-
200
,
,
9
,
.
100
?-
o
.
/
l i
0
,
,
,
9
,
*
*
.
,
/o
,
.~~'~
_sin"
9 * , 9 .0~.~-"
.
.
*
Rates of tooth movement
Figures 6 and 7 show changes in the rates of
movement in the first (Fig. 6) and second
(Fig. 7) molars following the insertion of an
elastic band between the teeth. The highest rates
of tooth movement were observed during the
initial hour following band insertion, in both
the first and second molars, in each of the
groups. The rates of movement in both the first
*
e-e~
o
9
,
..~0 S o ~
o~O ~ o ~
~. 9 o~O ~o~
~
9
,
9
9
9
O
E
* * :** * ,i
,
300
Differences between the control and the BAPN
groups, or between the control and the HC
groups were only significant at a few timepoints, as indicated in Figures 4 and 5. In
contrast, differences between the BAPN group
and the HC group, in both the first and second
molars, were all signi¡
The differences
between the first and second molars were als 9
examined; the average values at the end of the
experimental period were virtually identical in
the HC group (246+38 ~tm in the ¡
and
246_+44 ~tm in the second molar), slightly
greater (not significant) in the first (293_+
70 ~tm) than in the second (276 + 58 ~tm) molars
in the control group, and significantly greater
(P<0.05) in the first (348_+34 ~tm) than in the
second (306_+30 ~tm) molars in the BAPN
group.
~
o -o
*
o~O"
o
90
~.o ~
--o-- Saline
--e- BAPN
--.- HC
First m o l a r
c-
,
*
0_o
o""
0 ...'o f
~o ~
/r
9
i.
~
Ce 0 ~
,,,,0
~ o "~
91
10
0
E
_*.,1
_o.,..o " o"
II
f
~g.-~
C
9
E
I
I
I
I
5
10
15
20
Time after insertion of elastic band (hours)
Total movement (I.tm) of the reference points in
the second molar following the insertion of an elastic band
between the teeth, in rats which had received daily injections
of saline, 13-aminopropionitrile (BAPN) or hydrocortisone
(HC). The position of the reference point before band
insertion is labelled as 0. Each point represents the mean
of data collected from 9-12 animals. Significant differences
between the control and BAPN groups, *P<0.05,
* * P < 0 . 0 1 ; and between the BAPN and HC groups,
**P<0.01, ***P<0.001.
60
~ ~o
E
r
-"
O
30
0
I
Figure 5
amount of tooth movement, in both the first
(Fig. 4) and second (Fig. 5) molars, was largest
in the BAPN group, less in the control group,
and least in the HC group at any time-point.
Y-/O-o-"-o-S.-e
*o-'-.-.
~
a:
0
0
j
i
I
I
5
10
15
~/
20
T i m e a f t e r i n s e r t i o n o f e l a s t i c band ( h o u r s )
Figure 6
Rates of movement (~tm/h) of the reference points
in the first molar, following the insertion of ah e!astic band,
in rats which had received daily injections of saline,
[3-aminopropionitrile (BAPN) oc hydrocortisone (HC). The
position of the reference point before band insertion is
labelled as 0. Each point represents the mean of data
collected from 9-12 animals. Significant differences between
the control and BAPN groups, * P < 0 . 0 5 ; between the
control and HC groups, ~ P < 0 . 0 5 ; and between the BAPN
and HC groups, *P<0.05, **P<0.01.
26
A. YAMANE ET AL.
--o-- Saline
--e-- BAPN
--"-- HC
*
=
O
r-
..
90
Seconcl
molar
E
f..
~ 3o
0/o...
I
I[I
0
o-a-t~b"
~r
0
Time
after
,,,,?,ll====ll ='
L
i
I
I
5
10
15
20
of elastic
band (hours)
insertion
Figure 7 Rates of movement (pm/h) of the reference points
in the second molar, following the insertion of ah elastic
band, in rats which had received daily injections of saline,
13-aminopropionitrile (BAPN) or hydrocortisone (HC).
Position of the reference point before insertion of the band
is labelled as 0. Each point represents the mean of data
collected from 9 12 animals. Significant differences between
the control and BAPN groups, *-P<0.05, *4tP<0.01;
between the control and HC groups, ~/~rP<0.05,
~ ~ P < 0 . 0 1 ; and between the BAPN and HC groups,
*P <0.05, ***P<0.001.
and second molars, during the initial hour, were
highest in the BAPN group, lower in the control
group, and lowest in the HC group. However,
in all cases during the initial hour the rates were
higher in the second molars than in the first
molars. After the initial period, the rates
decreased gradually, without any marked
differences among the groups or between the
first and second molars.
Discussion
Previous reports have described instances of
weight loss in lathyritic animals, due to a reduction in food intake (Fry et al., 1962; Sarnat
and Sciaky, 1965; Berkovitz et al., 1972).
Lathyrogens have also been reported to cause
an increase in the weight of mandibles, by
inducing abnormal bone formation (exostosis)
(Marwah et al., 1963; Sarnat and Sciaky, 1965;
Koizumi, 1986; Kondo, 1991; Yamaguchi,
1992). However, in the present experiment,
there were no significant differences in the
weights of animals and mandibles between the
control group and the BAPN group (Table 1).
Previous studies have shown that the soft tissues
can be removed from mandibles completely and
reliable statistical evaluation of the mandible
weight can be obtained (Yamane, 1990; Yamane
et al., 1990).Therefore, it appears that systemic
reactions to the drug were minimal in the present experiment. Other research has shown that
glucocorticoids can lead to a reduction in body
weight and in the weight of the adrenal glands,
due to atrophy (Winter et al., 1950; Parmer
et al., 1951; Ball, 1977). Significant decreases in
the weights of animals and adrenal glands were
observed in the present study (Table 1), and in
previous experiments (Ohkawa, 1982; Yumoto,
1986), suggesting that hydrocortisone had a
noticeable systemic effect on the experimental
animals.
The time-lapse videotape method used to
monitor in vitro tooth movement has several
advantages: fixation of the jaw and determination of reference points are technically simple,
complex tooth movement can be recorded as
traces of the reference points, two-dimensional
tooth movement can be easily visualized, and
the images can all be stored on videotapes.
However, there are also several limitations and
problems inherent in this technique. The most
important problem is that in vitro results are
not directly applicable to in vivo conditions. In
the interpretation of in vitro results, various
biological factors affecting orthodontic tooth
movement, such as vasculature (Zaki and Van
Huysen, 1963; Kuitert et al., 1988, 1989), bone
resorption and apposition (Macapanpan et al.,
1954; Engstr6m et al., 1988; Tanaka et al.,
1990), and remodelling of periodontal fibres
(Azuma, 1970; Diaz, 1978), should be taken
into account. In addition, three-dimensional
tooth movement, tipping, and vertical movement (Macapanpan et al., 1954; Waldo and
Rothblatt, 1954; Zaki and Van Huysen, 1963;
Baumrind, 1969) cannot be recorded using this
technique. It is also assumed that the tooth
movement recorded might be caused not only
by deformation of the periodontal ligament but
also by that of the alveolar bone and tooth,
particularly when the magnitude of an orthodontic force was relatively great. Despite these
limitations, useful information could be
obtained regarding the complex orthodontic
tooth movements associated mainly with the
biomechanical properties of the periodontal
ligament.
Macapanpan et al. (1954) previously showed
that the rat maxillary first molar moved in a
IN VITRO ORTHODONTIC TOOTH MOVEMENT
mesiobuccal direction and the second and third
molars moved in a straight distal direction, after
a piece of rubber dam was inserted between the
first and second molars. In the present experiment, the rat mandibular ¡
molar also moved
in a mesiolingual direction, but the second
molar moved in a distobuccal direction (Fig. 3).
It is likely that the direction of orthodontic
tooth movement primarily reflects the direction
of the force applied to the teeth; thus the
discrepancies observed may result from structural differences between the maxillary and
mandibular molars.
The amount and rate of tooth movement was
highest during the initial hour after band insertion in both the first and second molars in all
of the groups (Figs. 4-7). Ohkawa (1982) suggested that the magnitude of force exerted on
the teeth by an elastic band decreases gradually
as the interdental space widens and the rubber
deteriorates; a force initially estimated to be a
few kilograms was eventually reduced to a few
hundred grams. The greatest tooth movement
in this study was observed during the time in
which the band was being inserted between the
teeth (,-~ 1-7 minutes). The tooth movement
during that period ranged from 61-96 per cent
of the total movement observed in the initial
hour. Therefore, it appears that the level of
force exerted on the teeth was greatest during
band insertion, rapidly and markedly decreased
soon after the procedure, and continued to
decrease gradually throughout the remaining
experimental period.
The total tooth movement throughout the
experimental period was greater in the ¡
molar than in the second molar in the BAPN
and control groups, but not in the H C group
(Figs. 4 and 5). Several previous studies have
shown that a tipping movement occurs in rat
molars following the insertion of an elastic band
between the teeth (Waldo and Rothblatt, 1954;
Zaki and Van Huysen, 1963; Baumrind, 1969).
The tipping movement probably contributes t o
the total amount of tooth movement and was
greater in the first molar than in the second
molar, particularly at the end of the experimental period in the control and BAPN groups.
The mean rate of tooth movement during the
initial hour was greater in the second than in
the first molars in all of the groups (Figs. 6 and
7). Macapanpan et al. (1954) have suggested
that the number, spatial arrangement, relative
27
strength, and divergence of the roots determine
movement in multi-rooted teeth. The rat mandibular first molar is larger than the second
molar and has four rather thick roots; the
second molar has four rather thin roots.
Therefore, the first molar may become more
firmly anchored to the alveolar bone than the
second molar when an orthodontic force is
applied.
Previous research has shown that the level of
soluble collagen in various connective tissues
increased (e.g. Smith and Shuster, 1962; Vogel,
1975; Taverne et al., 1986) and the mechanical
strength of the periodontal ligament of the rat
molar decreased, following the administration
of lathyrogens (Koizumi, 1986; Ohshima et al.,
1989; Kondo, 1991). In contrast, glucocorticoids have been shown to cause a decrease in saltsoluble collagen in the skin (Houck and Patel,
1965; Vogel, 1974) and an increase in the
mechanical strength of the periodontal ligament
in the rat molar (Ohkawa, 1982; Yumoto, 1986).
In the present experiment, BAPN accelerated
experimental tooth movement in vitro, whereas
tooth movement was inhibited by hydrocortisone (Figs. 3-7). From these results, it appears
that changes in the visco-elastic nature of the
periodontal ligament occurred a s a result of
changes in soluble and insoluble collagen content within the ligament, in rats which had
received daily injections of BAPN or hydrocortisone. Therefore, although a part of the tooth
movement recorded in this study might be
caused by the deformation of the alveolar bone,
the mechanical properties of the periodontal
ligament seem to play an important role in the
regulation of orthodontic tooth movement.
Address for correspondence
Dr. Akira Yamane
Department of Pharmacology, School of Dental
Medicine
Tsurumi University
2-1-3 Tsurumi, Tsurumi-ku
Yokohama, Japan 230
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